Cytotoxic necrotizing factors (CNFs)-a growing toxin family

Toxins

Volumn 2, Issue 1, 2010, Pages 116-127

  Knust, Zeynep ^a   Schmidt, Gudula ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Bacterial toxin; CNF; Deamidation; Rho GTPase activation

Indexed keywords

BACTERIAL TOXIN; CYTOTOXIC NECROTIZING FACTOR 1; CYTOTOXIC NECROTIZING FACTOR 2; CYTOTOXIC NECROTIZING FACTOR 3; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; YERSINIA CYTOTOXIC NECROTIZING FACTOR; CYTOTOXIN; ESCHERICHIA COLI PROTEIN;

BORDETELLA; DEAMINATION; ENZYME ACTIVATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; REVIEW; STREPTOMYCES GRISEUS; STRUCTURE ACTIVITY RELATION; YERSINIA PSEUDOTUBERCULOSIS; METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIAL TOXINS; CYTOTOXINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; RHO GTP-BINDING PROTEINS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 79952046248     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins2010116     Document Type: Review

References (59)

1. Villalonga, P.; Ridley, A.J. Rho GTPases and cell cycle control. Growth Factors 2006, 24, 159-164.
2. Aktories, K.; Schmidt, G.; Just, I. Rho GTPases as targets of bacterial protein toxins. Biol. Chem. 2000, 381, 421-426.
3. Caprioli, A.; Falbo, V.; Roda, L.G.; Ruggeri, F.M.; Zona, C. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun. 1983, 39, 1300-1306.
4. Foxman, B.; Zhang, L.; Palin, K.; Tallman, P.; Marrs, C.F. Bacterial virulence characteristics of Escherichia coli isolates from first-time urinary tract infection. J. Infect. Dis. 1995, 171, 1514-1521.
5. Foxman, B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am. J. Med. 2002, 113 Suppl 1A, 5S-13S.
6. Landraud, L.; Gauthier, M.; Boquet, P. Frequency of Escherichia coli strains producing the cytotoxic necrotizing factor (CNF1) in nosocomial urinary tract infections. Lett. Appl. Microbiol. 2000, 30, 213-216.
7. Yamamoto, S.; Tsukamoto, T.; Terai, A.; Kurazono, H.; Takeda, Y.; Yoshida, O. Distribution of virulence factors in Escherichia coli isolated from urine of cystitis patients. Microbiol. Immunol. 1995, 39, 401-404.
8. Rippere-Lampe, K.E.; O'Brien, A.D.; Conran, R.; Lockman, H.A. Mutation of the gene encoding cytotoxic necrotizing factor type 1 (cnf1) attenuates the virulence of uropathogenic Escherichia coli. Infect. Immun. 2001, 69, 3954-3964.
9. Fournout, S.; Dozois, C.M.; Odin, M.; Desautels, C.; Pérès, S.; Hérault, F.; Daigle, F.; Segafredo, C.; Laffitte, J.; Oswald, E.; Fairbrother, J.M.; Oswald, I.P. Lack of a role of cytotoxic necrotizing factor 1 toxin from Escherichia coli in bacterial pathogenicity and host cytokine response in infected germfree piglets. Infect. Immun. 2000, 68, 839-847.
10. Petkovsek, Z.; Elersic, K.; Gubina, M.; Zgur-Bertok, D.; Starcic, E.M. Virulence potential of Escherichia coli isolates from skin and soft tissue infections. J. Clin. Microbiol. 2009, 47, 1811-1817.
11. Khan, N.A.; Wang, Y.; Kim, K.J.; Chung, J.W.; Wass, C.A.; Kim, K.S. Cytotoxic necrotizing factor-1 contributes to Escherichia coli K1 invasion of the central nervous system. J. Biol. Chem. 2002, 277, 15607-15612.
12. Ananias, M.; Yano, T. Serogroups and virulence genotypes of Escherichia coli isolated from patients with sepsis. Braz. J. Med. Biol. Res. 2008, 41, 877-883.
13. Oswald, E.; de Rycke, J.; Guillot, J.F.; Boivin, R. Cytotoxic effect of multinucleation in HeLa cell cultures associated with the presence of Vir plasmid in Escherichia coli strains. FEMS Microbiol. Lett. 1989, 58, 95-100.
14. Orden, J.A.; Dominguez-Bernal, G.; Martinez-Pulgarin, S.; Blanco, M.; Blanco, J.E.; Mora, A.; checkentity /checkentity Blanco, J.; Blanco, J.; de la, F.R. Necrotoxigenic Escherichia coli from sheep and goats produce a new type of cytotoxic necrotizing factor (CNF3) associated with the eae and ehxA genes. Int. Microbiol. 2007, 10, 47-55.
15. Oswald, E.; de Rycke, J. A single protein of 110 kDa is associated with the multinucleating and necrotizing activity coded by the Vir plasmid of Escherichia coli. FEMS Microbiol. Lett. 1990, 68, 279-284.
16. Kadhum, H.J.; Finlay, D.; Rowe, M.T.; Wilson, I.G.; Ball, H.J. Occurrence and characteristics of cytotoxic necrotizing factors, cytolethal distending toxins and other virulence factors in Escherichia coli from human blood and faecal samples. Epidemiol. Infect. 2008, 136, 752-760.
17. Falzano, L.; Fiorentini, C.; Donelli, G.; Michel, E.; Kocks, C.; Cossart, P.; Cabanié, L.; Oswald, E.; Boquet, P. Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol. Microbiol. 1993, 9, 1247-1254.
18. Rippere-Lampe, K.E.; Lang, M.; Ceri, H.; Olson, M.; Lockman, H.A.; O'Brien, A.D. Cytotoxic necrotizing factor type 1-positive Escherichia coli causes increased inflammation and tissue damage to the prostate in a rat prostatitis model. Infect. Immun. 2001, 69, 6515-6519.
19. Hopkins, A.M.; Walsh, S.V.; Verkade, P.; Boquet, P.; Nusrat, A. Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J. Cell Sci. 2003, 116, 725-742.
20. Hofmann, P.; Le Negrate, G.; Mograbi, B.; Hofmann, V.; Brest, P.; Alliana-Schmid, A.; Flatau, G.; Boquet, P.; Rossi, B. Escherichia coli cytotoxic necrotizing factor-1 (CNF-1) increases the adherence to epithelia and the oxidative burst of human polymorphonuclear leukocytes but decreases bacteria phagocytosis. J. Leukoc. Biol. 2000, 68, 522-528.
21. Doye, A.; Mettouchi, A.; Bossis, G.; Clément, R.; Buisson-Touati, C.; Flatau, G.; Gagnoux, L.; Piechaczyk, M.; Boquet, P.; Lemichez, E. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 2002, 111, 553-564.
22. Lax, A.J. Bacterial toxins and cancer-A case to answer? Nat. Rev. Microbiol. 2005, 3, 343-349.
23. Miraglia, A.G.; Travaglione, S.; Meschini, S.; Falzano, L.; Matarrese, P.; Quaranta, M.G.; Viora, M.; Fiorentini, C.; Fabbri, A. Cytotoxic necrotizing factor 1 prevents apoptosis via the Akt/IkappaB kinase pathway: role of nuclear factor-kappaB and Bcl-2. Mol. Biol. Cell 2007, 18, 2735-2744.
24. Schmidt, G.; Sehr, P.; Wilm, M.; Selzer, J.; Mann, M.; Aktories, K. Gln63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor 1. Nature 1997, 387, 725-729.
25. Flatau, G.; Lemichez, E.; Gauthier, M.; Chardin, P.; Paris, S.; Fiorentini, C.; Boquet, P. Toxin- induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 1997, 387, 729-733.
26. Horiguchi, Y.; Nakai, T.; Kume, K. Purification and characterization of Bordetella bronchiseptica dermonecrotic toxin. Microb. Pathogen. 1989, 6, 361-368.
27. Masuda, M.; Betancourt, L.; Matsuzawa, T.; Kashimoto, T.; Takao, T.; Shimonishi, Y.; Horiguchi, Y. Activation of Rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin. EMBO J. 2000, 19, 521-530.
28. Schmidt, G.; Goehring, U.-M.; Schirmer, J.; Uttenweiler-Joseph, S.; Wilm, M.; Lohmann, M.; Giese, A.; Schmalzing, G.; Aktories, K. Lysine and polyamines are substrates for transglutamination of Rho by the Bordetella dermonecrotic toxin. Infect. Immun. 2001, 69, 7663-7670.
29. McNichol, B.A.; Rasmussen, S.B.; Meysick, K.C.; O'Brien, A.D. A single amino acid substitution in the enzymatic domain of cytotoxic necrotizing factor type 1 of Escherichia coli alters the tissue culture phenotype to that of the dermonecrotic toxin of Bordetella spp. Mol. Microbiol. 2006, 60, 939-950.
30. Schmidt, G.; Goehring, U.-M.; Schirmer, J.; Lerm, M.; Aktories, K. Identification of the C-terminal part of Bordetella dermonecrotic toxin as a transglutaminase for Rho GTPases. J. Biol. Chem. 1999, 274, 31875-31881.
31. Fiorentini, C.; Fabbri, A.; Flatau, G.; Donelli, G.; Matarrese, P.; Lemichez, E.; Falzano, L.; Boquet, P. Escherichia coli cytotoxic necrotizing factor 1 (CNF1), a toxin that activates the Rho GTPase. J. Biol. Chem. 1997, 272, 19532-19537.
32. Denko, N.; Langland, R.; Barton, M.; Lieberman, M.A. Uncoupling of S-phase and mitosis by recombinant cytotoxic necrotizing factor 2 (CNF2). Exp. Cell Res. 1997, 234, 132-138.
33. Malorni, W.; Fiorentini, C. Is the Rac GTPase-activating toxin CNF1 a smart hijacker of host cell fate? FASEB J. 2006, 20, 606-609.
34. Hoffmann, C.; Pop, M.; Leemhuis, J.; Schirmer, J.; Aktories, K.; Schmidt, G. The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J. Biol. Chem. 2004, 279, 16026-16032.
35. Sugai, M.; Hatazaki, K.; Mogami, A.; Ohta, H.; Pérès, S.Y.; Hérault, F.; Horiguchi, Y.; Masuda, M.; Ueno, Y.; Komatsuzawa, H.; Suginaka, H.; Oswald, E. Cytotoxic necrotizing factor type 2 produced by pathogenic Escherichia coli deamidates a Gln residue in the conserved G-3 domain of the Rho family and preferentially inhibits the GTPase activity of RhoA and Rac1. Infect. Immun. 1999, 67, 6550-6557.
36. Stoll, T.; Markwirth, G.; Reipschlager, S.; Schmidt, G. A new member of a growing toxin family- Escherichia coli cytotoxic necrotizing factor 3 (CNF3). Toxicon 2009, 54, 745-753.
37. Lerm, M.; Pop, M.; Fritz, G.; Aktories, K.; Schmidt, G. Proteasomal degradation of cytotoxic necrotizing factor 1-activated Rac. Infect. Immun. 2002, 70, 4053-4058.
38. Munro, P.; Flatau, G.; Doye, A.; Boyer, L.; Oregioni, O.; Mege, J.L.; Landraud, L.; Lemichez, E. Activation and proteasomal degradation of Rho GTPases by CNF1 elicit a controlled inflammatory response. J. Biol. Chem. 2004, 279, 35849-35857.
39. Pop, M.; Aktories, K.; Schmidt, G. Isotype-specific degradation of Rac activated by the cytotoxic necrotizing factor 1 (CNF1). J. Biol. Chem. 2004, 279, 35840-35848.
40. Lemichez, E.; Flatau, G.; Bruzzone, M.; Boquet, P.; Gauthier, M. Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol. Microbiol. 1997, 24, 1061-1070.
41. Schmidt, G.; Selzer, J.; Lerm, M.; Aktories, K. The Rho-deamidating cytotoxic-necrotizing factor CNF1 from Escherichia coli possesses transglutaminase activity - cysteine-866 and histidine-881 are essential for enzyme activity. J. Biol. Chem. 1998, 273, 13669-13674.
42. Buetow, L.; Flatau, G.; Chiu, K.; Boquet, P.; Ghosh, P. Structure of the Rho-activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat. Struct. Biol. 2001, 8, 584-588.
43. Hoffmann, C.; Aktories, K.; Schmidt, G. Change in substrate specificity of Cytotoxic Necrotizing Factor (CNF) unmasks proteasome-independent down-regulation of constitutively active RhoA. J. Biol. Chem. 2007, 282, 10826-10832.
44. Buetow, L.; Ghosh, P. Structural elements required for deamidation of RhoA by cytotoxic necrotizing factor 1. Biochemistry 2003, 42, 12784-12791.
45. Contamin, S.; Galmiche, A.; Doye, A.; Flatau, G.; Benmerah, A.; Boquet, P. The p21 Rho activating toxin cytotoxic necrotizing factor 1 is endocytosed by a clathrin-independent mechanism and enters the cytosol by an acidic-dependent membrane translocation step. Mol. Biol. Cell 2000, 11, 1775-1787.
46. Fabbri, A.; Gauthier, M.; Boquet, P. The 5' region of cnf1 harbours a translational regulatory mechanism for CNF1 synthesis and encodes the cell-binding domain of the toxin. Mol Microbiol 1999, 33, 108-118.
47. Chung, J.W.; Hong, S.J.; Kim, K.J.; Goti, D.; Stins, M.F.; Shin, S.; Dawson, V.L.; Dawson, T.M.; Kim, K.S. 37 kDa laminin receptor precusor modulates cytotoxic necrotizing factor 1-mediated RhoA activation and bacterial uptake. J. Biol. Chem. 2003, 278, 16857-16862.
48. Kim, K.J.; Chung, J.W.; Kim, K.S. 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J. Biol. Chem. 2005, 280, 1360-1368.
49. Blumenthal, B.; Hoffmann, C.; Aktories, K.; Backert, S.; Schmidt, G. The Cytotoxic Necrotizing Factors from Yersinia pseudotuberculosis and from Escherichia coli Bind to Different Cellular Receptors but Take the Same Route to the Cytosol. Infect. Immun. 2007, 75, 3344-3353.
50. McNichol, B.A.; Rasmussen, S.B.; Carvalho, H.M.; Meysick, K.C.; O'Brien, A.D. Two domains of cytotoxic necrotizing factor type 1 bind the cellular receptor, laminin receptor precursor protein. Infect. Immun. 2007, 75, 5095-5104.
51. Werner, G.; Hagenmaier, H.; Drautz, H.; Baumgartner, A.; Zahner, H. Metabolic products of microorganisms. 224. Bafilomycins, a new group of macrolide antibiotics. Production, isolation, chemical structure and biological activity. J. Antibiotics 1984, 37, 110-117.
52. Pei, S.; Doye, A.; Boquet, P. Mutation of specific acidic residues of the CNF1 T domain into lysine alters cell membrane translocation of the toxin. Mol. Microbiol. 2001, 41, 1237-1247.
53. O'Keefe, D.O.; Cabiaux, V.; Choe, S.; Eisenberg, D.; Collier, R.J. PH-dependent insertion of proteins into membranes: B-chain mutation of diphtheria toxin inhibits membrane translocation, Glu-349» Lys. Proc. Natl. Acad. Sci. USA 1992, 89, 6202-6206.
54. Knust, Z.; Blumenthal, B.; Aktories, K.; Schmidt, G. Cleavage of Escherichia coli cytotoxic necrotizing factor 1 is required for full biologic activity. Infect. Immun. 2009, 77, 1835-1841.
55. Kouokam, J.C.; Wai, S.N.; Fallman, M.; Dobrindt, U.; Hacker, J.; Uhlin, B.E. Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect. Immun. 2006, 74, 2022-2030.
56. Davis, J.M.; Carvalho, H.M.; Rasmussen, S.B.; O'Brien, A.D. Cytotoxic necrotizing factor type 1 delivered by outer membrane vesicles of uropathogenic Escherichia coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis. Infect. Immun. 2006, 74, 4401-4408.
57. Yu Hao; Kim, K.S. Ferredoxin is involved in secretion of cytotoxic necrotizing factor 1 across the cytoplasmic membrane in Escherichia coli K1. Infect. Immun. 2009, doi.10.1128/IAI.00674-09.
58. Diana, G.; Valentini, G.; Travaglione, S.; Falzano, L.; Pieri, M.; Zona, C.; Meschini, S.; Fabbri, A.; Fiorentini, C. Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc. Natl. Acad. Sci. USA 2007, 104, 636-641.
59. Pavone, F.; Luvisetto, S.; Marinelli, S.; Straface, E.; Fabbri, A.; Falzano, L.; Fiorentini, C.; Malorni, W. The Rac GTPase-activating bacterial protein toxin CNF1 induces analgesia up- regulating mu-opioid receptors. Pain 2009, 145, 219-229.